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Promiscuous birds challenge the idea that more sexual partners speeds up evolution

Stuart Wigby, BBSRC David Phillips Research Fellow in the Department of Zoology, writes about new research on this subject in an article first published in the Conversation.

Zsuzsa Ákos

Females are coy and males are ardent. This was Darwin’s somewhat Victorian portrayal of the sexes in his book 'The Descent of Man and Selection in Relation to Sex'. The myth that males are naturally promiscuous and females naturally monogamous, persisted for a century after Darwin’s book was published, becoming perhaps his least helpful legacy.

In reality, monogamy is relatively rare in nature, for either sex. Towards the end of the 20th century, scientists began to take a renewed interest in sexual selection. The advent of genetic tests for paternity revealed that female animals were actually having plenty of sex, and with lots of males.

Perhaps the most surprising finding was that many bird species that look monogamous at first glance – they build nests together and cooperate in raising offspring – were actually mating all over the place, such that broods often contained many half-siblings. Darwin’s contemporaries would have been shocked.

In the wild, then, it seems that promiscuity is rife – and this has important consequences for evolution. The traditional thinking is that promiscuity intensifies sexual selection, an evolutionary process whereby individuals develop traits that help them gain more mates and offspring. This should speed up evolution, leading to the rapid formation of new species (speciation). But a new study on shorebirds from researchers at the University of Bath suggests the exact opposite. So, what do we really know about the link between sex and speciation?

Fights and fancy ornaments

Darwin’s original ideas about sexual selection were based largely on males competing for mates, either by fighting among themselves or by showing off fancy ornaments to attract choosy females. And it is indeed likely that sexual selection led to the evolution of stags’ antlers and male peacocks’ tails.

But when females are promiscuous, sexual selection gets even more interesting. If a female mates with different males in quick succession then the sperm of those males compete for the female’s eggs. This is one of the reasons that the males of many species have evolved to produce large numbers of sperm: they’re tickets in the fertilisation raffle.

Promiscuity can also mean conflict. Whereas lifelong monogamous couples have completely shared interests, short-term relationships can quickly turn sour. For example, promiscuity can lead to the evolution of sinister means of preventing your mates reproducing with a rival, or guarding against unwanted attention. Adaptations include medieval-looking spiky penises in seed beetles, toxic seminal fluid in flies, and defensive spines on female water striders.

But what does all this mean for the evolutionary tree of life? Does more sex mean more species? Broadly speaking the view has been yes. More sex equals more selection, which equals rapid evolution and so more species. The thinking is that an evolutionary to-and-fro between the sexes – male ornaments evolving with female preferences, or harmful male traits evolving with female defences – can lead to rapid cycles of evolution. This leads to quickly differentiating populations and stops them interbreeding.

Some past studies support these ideas and find female promiscuity is associated with higher speciation rates, although other studies find little evidence for this. However, a new study published in Evolution suggests the exact opposite. The data shows that in shorebirds, there are more subspecies (races) among monogamous species than among more promiscuous species. So what’s going on here?

The study authors, led by Josephine D'Urban Jackson, suggest that the answer lies in promiscuous birds dispersing in search of more mates. More dispersal means that populations mix freely and exchange genes. This makes it less likely for sexual selection to produce different traits in different populations, so reducing the chance of a completely new species evolving. In contrast, monogamous couples move around less, and mate within a more local pool of birds. This allows populations to genetically diverge over time, eventually becoming different species.

Measuring sexual selection

So, does this then mean that sexual selection does not in fact drive speciation? Not necessarily. In general, sexual selection is stronger when some individuals in a species are better than others at attracting mates and having lots of offspring. To measure this directly, you need to know how many mates and offspring everyone has, which – as you might imagine – is not easy data to gather, especially in the wild.

Studies such as this new one use proxy measures, such as the degree of promiscuity, while other use male testes size, or sex differences in body size, to infer differences in the strength of sexual selection between species. But while promiscuity clearly opens the door to different aspects of sexual selection (such as dispersing to find additional mates) it does not necessarily increase the overall strength of sexual selection.

In fact, under some conditions sexual selection is weaker when females are promiscuous. This is because female promiscuity stops a minority of males from monopolising access to mating, and so all males have a more similar degree of success.

So, promiscuity probably alters the type of sexual selection acting on shorebirds, and it is certainly associated with reduced species diversity. But the broader debate over the relationship between sexual selection and speciation won’t be settled any time soon.

Stuart Wigby, BBSRC David Phillips Research Fellow, Department of Zoology